ALK4 functions as a receptor for multiple TGFβ-related ligands to regulate left-right axis determination and mesoderm induction in Xenopus

Developmental Biology

Volumn 268, Issue 2, 2004, Pages 280-294

  Chen, Yumei ^a   Mironova, Ekaterina ^b   Whitaker, Lisha L ^b   Edwards, Laura ^b,c   Yost, H Joseph ^d   Ramsdell, Ann F ^a,b,c  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b UNIVERSITY OF SOUTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF SOUTH CAROLINA   (United States)

^d UNIVERSITY OF UTAH   (United States)

Author keywords

ActRIB; ALK4; Derriere; Heterotaxy; Left right asymmetry; Nodal; TGF ; Vg1; Xnr1

Indexed keywords

ACTIVIN LIKE KINASE 4; ANTISENSE OLIGONUCLEOTIDE; ENZYME; HOMEODOMAIN PROTEIN; PROTEIN; PROTEIN DERRIERE; PROTEIN NODAL; PROTEIN NODAL RELATED 1; PROTEIN VG1; TRANSCRIPTION FACTOR PITX2; TRANSFORMING GROWTH FACTOR; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CHEMICAL ANALYSIS; CONTROLLED STUDY; EMBRYO; EMBRYO AXIS; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; FEMALE; GASTRULATION; IMMUNOPRECIPITATION; MESODERM; NONHUMAN; ORGANOGENESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; SIGNAL TRANSDUCTION; XENOPUS;

XENOPUS;

EID: 1942518341     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2003.12.035     Document Type: Article

References (73)

1. Agius E., Oelgeschlager M., Wessely O., Kemp C., De Robertis E.M. Endodermal Nodal-related signals and mesoderm induction in Xenopus. Development. 127:2000;1173-1183.
2. Armes N.A., Smith J.C. The ALK-2 and ALK-4 activin receptors transduce distinct mesoderm-inducing signals during early Xenopus development but do not co-operate to establish thresholds. Development. 124:1997;3797-3804.
3. Attisano L., Wrana J.L. Signal transduction by the TGF-beta superfamily. Science. 296:2002;1646-1647.
4. Branford W.W., Essner J.J., Yost H.J. Regulation of gut and heart left-right asymmetry by context-dependent interactions between Xenopus lefty and BMP4 signaling. Dev. Biol. 223:2000;291-306.
5. Campione M., Steinbeisser H., Schweickert A., Deissler K., van Bebber F., Lowe L.A., Nowotschin S., Viebahn C., Haffter P., Kuehn M.R., Blum M. The homeobox gene Pitx2: mediator of asymmetric left-right signaling in vertebrate heart and gut looping. Development. 126:1999;1225-1234.
6. Capdevila J., Vogan K.J., Tabin C.J., Izpisua Belmonte J.C. Mechanisms of left-right determination in vertebrates. Cell. 101:2000;9-21.
7. Chang C., Wilson P.A., Mathews L.S., Hemmati-Brivanlou A. A Xenopus type I activin receptor mediates mesodermal but not neural specification during embryogenesis. Development. 124:1997;827-837.
8. Cheng A.M., Thisse B., Thisse C., Wright C.V. The lefty-related factor Xatv acts as a feedback inhibitor of nodal signaling in mesoderm induction and L-R axis development in Xenopus. Development. 127:2000;1049-1061.
9. Cheng S.K., Olale F., Bennett J.T., Brivanlou A.H., Schier A.F. EGF-CFC proteins are essential coreceptors for the TGF-beta signals Vg1 and GDF1. Genes Dev. 17:2003;31-36.
10. Collignon J., Varlet I., Robertson E.J. Relationship between asymmetric nodal expression and the direction of embryonic turning. Nature. 381:1996;155-158.
11. Conlon F.L., Lyons K.M., Takaesu N., Barth K.S., Kispert A., Herrmann B., Robertson E.J. A primary requirement for nodal in the formation and maintenance of the primitive streak in the mouse. Development. 120:1994;1919-1928.
12. Dale L., Matthews G., Tabe L., Colman A. Developmental expression of the protein product of Vg1, a localized maternal mRNA in the frog Xenopus laevis. EMBO J. 8:1989;1057-1065.
13. Dale L., Matthews G., Colman A. Secretion and mesoderm-inducing activity of the TGF-beta-related domain of Xenopus Vg1. EMBO J. 12:1993;4471-4480.
14. Dohrmann C.E., Kessler D.S., Melton D.A. Induction of axial mesoderm by zdvr-1, the zebrafish orthologue of Xenopus Vg1. Dev. Biol. 175:1996;108-117.
15. Eimon P.M., Harland R.M. Effects of heterodimerization and proteolytic processing on Derriere and Nodal activity: implications for mesoderm induction in Xenopus. Development. 129:2002;3089-3103.
16. Frisch A., Wright C. XBMPRII, a novel Xenopus type II receptor mediating BMP signaling in embryonic tissues. Dev. Suppl. 125:1998;431-442.
17. Gray P.C., Greenwald J., Blount A.L., Kunitake K.S., Donaldson C.J., Choe S., Vale W. Identification of a binding site on the type II activin receptor for activin and inhibin. J. Biol. Chem. 275:2000;3206-3212.
18. Gritsman K., Zhang J., Cheng S., Heckscher E., Talbot W.S., Schier A.F. The EGF-CFC protein one-eyed pinhead is essential for nodal signaling. Cell. 97:1999;121-132.
19. Gu Z.Y., Nomura M., Simpson B.B., Lei H., Feijen A., van den Eijnden-van Raaij J., Donahoe P.K., Li E. The type I activin receptor ActRIB is required for egg cylinder organization and gastrulation in the mouse. Genes Dev. 12:1998;844-857.
20. Hanafusa H., Masuyama N., Kusakabe M., Shibuya H., Nishida E. The TGF-beta family member derriere is involved in regulation of the establishment of left-right asymmetry. EMBO Rep. 1:2000;32-39.
21. Hanafusa H., Masuyama N., Kusakabe M., Shibuya H., Nishida E. The TGF-beta family member derriere is involved in regulation of the establishment of left-right asymmetry. EMBO Rep. 1:2000;32-39.
22. Hemmati-Brivanlou A., Melton D.A. A truncated activin receptor inhibits mesoderm induction and formation of axial structures in Xenopus embryos. Nature. 359:1992;609-614.
23. Hyatt B.A., Yost H.J. The left-right coordinator: the role of Vg1 in organizing left-right axis formation. Cell. 93:1998;37-46.
24. Hyatt B.A., Lohr J.L., Yost H.J. Initiation of vertebrate left-right axis formation by maternal vg1. Nature. 384:1996;62-65.
25. Jones C.M., Kuehn M.R., Hogan B., Smith J.C., Wright C.V.E. Nodal-related signals induce axial mesoderm and dorsalize mesoderm during gastrulation. Development. 121:1995;3651-3662.
26. Joseph E.M., Douglas A.M. Mutant Vg1 ligands disrupt endoderm and mesoderm formation in Xenopus embryos. Development. 125:1998;2677-2685.
27. Kao K.R., Elinson R.P. The entire mesodermal mantle behaves as Spemann's organizer in dorsoanterior enhanced Xenopus laevis embryos. Dev. Biol. 127:1988;64-77.
28. Kathiriya I.S., Srivastava D. Left-right asymmetry and cardiac looping: implications for cardiac development and congenital heart disease. Am. J. Med. Genet. 97:2000;271-279.
29. Kessler D.S., Melton D.A. Induction of dorsal mesoderm by soluble, mature vg1 protein. Development. 121:1995;2155-2164.
30. Kramer K.L., Yost H.J. Ectodermal syndecan-2 mediates left-right axis formation in migrating mesoderm as a cell-nonautonomous Vg1 cofactor. Dev. Cell. 2:2002;115-124.
31. Kramer K.L., Barnette J.E., Yost H.J. PKCgamma regulates syndecan-2 inside-out signaling during Xenopus left-right development. Cell. 111:2002;981-990.
32. Lee M.A., Heasman J., Whitman M. Timing of endogenous activin-like signals and regional specification of the Xenopus embryo. Development. 126:2001;2939-2952.
33. Levin M. Left-right asymmetry and the chick embryo. Semin. Cell Dev. Biol. 9:1998;67-76.
34. Levin M., Johnson R.L., Stern C.D., Kuehn M., Tabin C. A molecular pathway determining left-right asymmetry in chick embryogenesis. Cell. 82:1995;803-814.
35. Levin M., Pagan S., Roberts D.J., Cooke J., Kuehn M.R., Tabin C.J. Left/right patterning signals and the independent regulation of different aspects of situs in the chick embryo. Dev. Biol. 189:1997;57-67.
36. Logan M., Pagan-Westphal S.M., Smith D.M., Paganessi L., Tabin C.J. The transcription factor Pitx2 mediates situs-specific morphogenesis in response to left-right asymmetric signals. Cell. 94:1998;307-317.
37. Lohr J.L., Danos M.C., Yost H.J. Left-right asymmetry of a nodal-related gene is regulated by dorsoanterior midline structures during Xenopus development. Development. 124:1997;1465-1472.
38. Lohr J.L., Danos M.C., Groth T.W., Yost H.J. Maintenance of asymmetric nodal expression in Xenopus laevis. Dev. Genet. 23:1998;194-1202.
39. Lowe L.A., Supp D.M., Sampath K., Yokoyama T., Wright C.V.E., Potter S.S., Overbeek P., Kuehn M.R. Conserved left-right asymmetry of nodal expression and alterations in murine situs inversus. Nature. 381:1996;158-161.
40. Massague J. TGF-beta signal transduction. Annu. Rev. Biochem. 67:1998;753-791.
41. Matzuk M.M., Kumar T.R., Vassalli A., Bickenbach J.R., Roop D.R., Jaenisch R., Bradley A. Functional analysis of activins during mammalian development. Nature. 374:1995;354-356.
42. Mercola M., Levin M. Left-right asymmetry determination in vertebrates. Annu. Rev. Cell Dev. Biol. 17:2001;779-805.
43. Murphy-Ullrich J.E., Poczatek M. Activation of latent TGF-beta by thrombospondin-1: mechanisms and physiology. Cytokine Growth Factor Rev. 11:2000;59-69.
44. Nagaso H., Suzuki A., Tada M., Ueno N. Dual specificity of activin type II receptor ActRIIb in dorso-ventral patterning during zebrafish embryogenesis. Dev. Growth Differ. 41:1999;119-133.
45. Nieuwkoop P.D., Faber J. Normal Table of Xenopus laevis (Daudin). 1967;North-Holland, Amsterdam.
46. Nomura M., Li E. Smad2 role in mesoderm formation, left-right patterning and craniofacial development. Nature. 393:1998;786-790.
47. Oh S.P., Li E. The signaling pathway mediated by the type IIB activin receptor controls axial patterning and lateral asymmetry in the mouse. Genes Dev. 11:1997;1812-1826.
48. Piedra M.E., Icardo J.M., Albajar M., Rodriguez-Rey J.C., Ros M.A. Pitx2 participates in the late phase of the pathway controlling left-right asymmetry. Cell. 94:1998;319-324.
49. Ramsdell A.F., Yost H.J. Molecular mechanisms of vertebrate left-right development. Trends Genet. 14:1998;459-465.
50. Ramsdell A.F., Yost H.J. Cardiac looping and the left-right axis: antagonism of left-sided Vg1 activity by a right-sided ALK2-dependent BMP pathway. Development. 126:1999;5195-5205.
51. Ramsdell A.F., Yost H.J. Cardiac looping and the left-right axis: integrating morphological, molecular, and genetic analyses of vertebrate left-right asymmetry. Tomanek R.J., Runyan R.B. Formation of the Heart and its Regulation. 2001;45-73 Birkhäuser, Boston, MA.
52. Rankin C.T., Bunton T., Lawler A.M., Lee S.J. Regulation of left-right patterning in mice by growth/differentiation factor-1. Nat. Genet. 24:2000;262-265.
53. Reissmann E., Jornvall H., Blokzijl A., Andersson O., Chang C., Minchiotti G., Persico M.G., Ibanez C.F., Brivanlou A.H. The orphan receptor ALK7 and the activin receptor ALK4 mediate signaling by nodal proteins during vertebrate development. Genes Dev. 15:2001;1-14.
54. Sakuma R., Ohnishi Yi Y., Meno C., Fujii H., Juan H., Takeuchi J., Ogura T., Li E., Miyazono K., Hamada H. Inhibition of Nodal signalling by Lefty mediated through interaction with common receptors and efficient diffusion. Genes Cells. 7:2002;401-412.
55. Sampath K., Cheng A.M., Frisch A., Wright C.V. Functional differences among Xenopus nodal-related genes in left-right axis determination. Development. 124:1997;3293-3302.
56. Schier A.F., Shen M.M. Nodal signalling in vertebrate development. Nature. 403:2000;385-389.
57. Schulte-Merker S., Smith J.C., Dale L. Effects of truncated activin and FGF receptors and of follistatin on the inducing activities of BVg1 and activin: does activin play a role in mesoderm induction? EMBO J. 13:1994;3533-3541.
58. Seleiro E.A., Connolly D.J., Cooke J. Early developmental expression and experimental axis determination by the chicken Vg1 gene. Curr. Biol. 6:1996;1476-1486.
59. Shah S.B., Skromne I., Hume C.R., Kessler D.S., Lee K.J., Stern C.D., Dodd J. Misexpression of chick Vg1 in the marginal zone induces primitive streak formation. Development. 124:1997;5127-5138.
60. Shen M.M., Schier A.F. The EGF-CFC gene family in vertebrate development. Trends Genet. 16:2000;303-309.
61. Sun B.I., Bush S.M., Collins-Racie L.A., LaVallie E.R., DiBlasio-Smith E.A., Wolfman N.M., McCoy J.M., Sive H.L. Derriere: a TGFβ family member required for posterior development in Xenopus. Development. 126:1999;1467-1482.
62. Tannahill D., Melton D.A. Localized synthesis of the Vg1 protein during early Xenopus development. Development. 106:1989;775-785.
63. Thomsen G.H., Melton D.A. Processed Vg1 protein is an axial mesoderm inducer in Xenopus. Cell. 74:1993;433-441.
64. Ulloa L., Creemers J.W., Roy S., Liu S., Mason J., Tabibzadeh S. Lefty proteins exhibit unique processing and activate the MAPK pathway. J. Biol. Chem. 276:2001;21387-21396.
65. Wall N.A., Craig E.J., Labosky P.A., Kessler D.S. Mesendoderm induction and reversal of left-right pattern by mouse Gdf1, a Vg1-related gene. Dev. Biol. 227:2000;495-509.
66. Weeks D.L., Melton D.A. A maternal mRNA localized to the vegetal hemisphere in Xenopus eggs codes for a growth factor related to TGF-beta. Cell. 51:1987;861-867.
67. Whitman M. Smads and early developmental signaling by the TGFbeta superfamily. Genes Dev. 12:1998;2445-2462.
68. Whitman M., Mercola M. TGF-beta superfamily signaling and left-right asymmetry. Sci. STKE. 2001:2001;. Jan 9(64): RE1.
69. Wilson P.A., Hemmati-Brivanlou A. Induction of epidermis and inhibition of neural fate by Bmp-4. Nature. 376:1995;331-333.
70. Yan Y.T., Liu J.J., Luo Y.E.C., Haltiwanger R.S., Abate-Shen C., Shen M.M. Dual roles of Cripto as a ligand and coreceptor in the nodal signaling pathway. Mol. Cell. Biol. 22:2002;4439-4449.
71. Yeo C., Whitman M. Nodal signals to Smads through Cripto-dependent and Cripto-independent mechanisms. Mol. Cell. 7:2001;949-957.
72. Yoshioka H., Meno C., Koshiba K., Sugihara M., Itoh H., Ishimaru Y., Inoue T., Ohuchi H., Semina E.V., Murray J.C., Hamada H., Noji S. Pitx2, a bicoid-type homeobox gene, is involved in a lefty-signaling pathway in determination of left-right asymmetry. Cell. 94:1998;299-305.
73. Zhang J., Talbot W.S., Schier A.F. Positional cloning identifies zebrafish one-eyed pinhead as a permissive EGF-related ligand required during gastrulation. Cell. 92:1998;241-251.